Summary
The distribution of several extracellular matrix macromolecules was investigated at the myotendinous junction of adult chicken gastrocnemius muscle. Localization using monoclonal antibodies specific for 3 basal lamina components (type IV collagen, laminin, and a basement membrane form of heparan sulfate proteoglycan) showed strong fluorescent staining of the myotendinous junction for heparan sulfate proteoglycan and laminin, but not for type IV collagen. In addition, a strong fluorescent stain was observed at the myotendinous junction using a monoclonal antibody against the β subunit of the chicken integrin complex (antibody JG 22). Neither fibronectin nor tenascin were concentrated at the myotendinous junction, but instead were present in a fibrillar staining pattern throughout the connective tissue which was closely associated with the myotendinous junction. Tenascin also gave bright fluorescent staining of tendon, but no detectable staining of the perimysium or endomysium. Type I collagen was observed throughout the tendon and in the perimysium, but only faintly in the endomysium. In contrast, type III collagen was present brightly in the endomysium and in the perimysium, but could not be detected in the tendon except when associated with blood vessels and in the epitendineum, which stained intensely. Type VI collagen was found throughout the tendon and in all connective tissue partitions of skeletal muscle. The results indicate that one or more molecules of the integrin family may play an important role in the attachment of muscle to the tendon. This interaction does not appear to involve extensive binding to fibronectin or tenascin, but may involve laminin and heparan sulfate proteoglycan.
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Anderson MJ, Fambrough DM (1983) Aggregates of acetylcholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle fibers. J Cell Biol 97:1396–1411
Bayne EK, Anderson MJ, Fambrough DM (1984) Extracellular matrix organization in developing muscle: Correlation with acetylcholine receptor aggregates. J Cell Biol 99:1486–1501
Bogaert T, Brown N, Wilcox M (1987) The Drosophila PS2 antigen is an invertebrate integrin that like the fibronectin receptor, becomes localized to muscle attachments. Cell 51:929–940
Bruns RR, Press W, Engvall E, Timpl R, Gross J (1986) Type VI collagen in extracellular, 100-nm periodic filaments and fibrils: Identification by immunoelectron microscopy. J Cell Biol 103:393–404
Burridge K (1986) Substrate adhesions in normal and transformed fibroblasts: Organization and regulation of cytoskeletal, membrane and extracellular matrix components at focal contacts. Cancer Rev 4:18–78
Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: Origin of the limb musculature. J Embryol Exp Morphol 41:245–258
Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 98:1926–1936
Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: An extracellular matrix protein involved in tissue reactions during fetal development and oncogenesis. Cell 47:131–139
Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186
Couchman JR, Hook M, Rees DA, Timpl R (1983) Adhesion, growth and matrix production by fibroblasts on laminin substrate. J Cell Biol 96:177–183
Daniloff JK, Crossin KL, Pinson-Raymond M, Murawsky M, Rieger F, Edelman GM (1989) Expression of cytotactin in the normal and regenerating neuro-muscular system. J Cell Biol 108:625–635
Erickson HP, Lightner AV (1988) Hexabrachion protein (tenascin, cytotactin, brachionectin) in connective tissues, embryonic brain, and tumors. In: Miller KE (ed) Advances in Cell Biology, Vol. 2., JAI Press, pp 55–90
Gardner JM, Fambrough DM (1983) Fibronectin expression during myogenesis. J Cell Biol 96:474–485
Graf J, Iwamoto Y, Sasaki M, Martin GR, Kleinman HR, Robey FA, Yamada Y (1987) Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell 48:989–996
Greve JM, Gottlieb DJ (1982) Monoclonal antibodies which alter the morphology of cultured myogenic cells. J Cell Biochem 18:221–229
Hemler ME, Crouse C, Takada Y, Sonnenberg A (1988) Multiple very late antigen (VLA) heterodimers on platelets. J Biol Chem 263:7660–7665
Horwitz AF, Duggan K, Greggs R, Decker C, Buck C (1985) The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol 101:2134–2144
Horwitz AF, Duggan K, Buck C, Beckerle MC, Burridge K (1986) Interaction of plasma membrane fibronectin receptor with talin — a transmembrane linkage. Nature 320:531–533
Hynes RO (1987) Integrins: A family of cell surface receptors. Cell 48:549–554
Ishikawa H (1965) The fine structure of myotendon junction in some mammalian skeletal muscle. Arch Histol Jpn 25:275–296
Keene DR, Sakai LY, Bächinger HP, Burgeson RE (1987) Type III collagen can be present on banded collagen fibrils regardless of fibril diameter. J Cell Biol 105:2393–2402
Kieny M, Chevallier A (1979) Autonomy of tendon development in the embryonic chick wing. J Embryol Exp Morphol 49:153–165
Kühl U, Öcalan M, Timpl R, Mayne R, Hay E, von der Mark K (1984) Role of muscle fibroblasts in the deposition of type IV collagen in the basal lamina of myotubes. Differentiation 28:164–172
Leptin M, Aebersold R, Wilcox M (1987) Drosophila position-specific antigens resemble the vertebrate fibronectin-receptor family. EMBO J 6:1037–1043
Linsenmayer TF, Gibney E, Fitch JM (1986a) Embryonic avian cornea contains layers of collagen with greater than average stability. J Cell Biol 103:1587–1593
Linsenmayer TF, Mentzer A, Irwin MH, Waldrep NK, Mayne R (1986b) Avian type VI collagen: Monoclonal antibody production and immunohistochemical identifications as a major connective tissue component of cornea and skeletal muscle. Exp Cell Res 165:518–529
Lubińska L, Zelená J (1967) Acetylcholinesterase at muscle — ten-don junctions during postnatal development in rats. J Anat 101:295–308
MacKrell AJ, Blumberg B, Haynes SR, Fessler JH (1988) The lethal myospheroid gene of Drosophila encodes a membrane protein homologous to vertebrate integrin β subunits. Proc Natl Acad Sci USA 85:2633–2637
Maier A, Mayne R (1987) Distribution of connective tissue proteins in chick muscle spindles as revealed by monoclonal antibodies: A unique distribution of brachionectin/tenascin. Am J Anat 180:226–236
Mayne R, Sanderson RD, Wiedemann H, Fitch JM, Linsenmayer TF (1983) The use of monoclonal antibodies to fragments of chicken type IV collagen in structural and localization studies. J Biol Chem 258:5794–579
Moore MJ (1983) The dual connective tissue system of rat soleus muscle. Muscle & Nerve 6:416–422
Neff NT, Lowrey C, Decker C, Tovar A, Damsky C, Buck C, Horwitz AF (1982) A monoclonal antibody detaches embryonic skeletal muscle from extracellular matrices. J Cell Biol 95:654–666
Ruoslahti E, Pierschbacher MD (1987) New perspectives in cell adhesion: RGD and integrins. Science 238:491–497
Shear CR, Bloch RJ (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: Localization and relationship to intracellular and extracellular structures. J Cell Biol 101:240–256
Shellswell GB, Wolpert L (1977) The pattern of muscle and tendon development in the chick wing. In: Ede DA, Hinchliffe JR, Balls M (eds) Vertebrate limb and somite morphogenesis. Cambridge University Press, London, pp 77–86
Tamkun JW, DeSimone DW, Fonda D, Patel RS, Buck C, Horwitz AF, Hynes RO (1986) Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell 46:271–282
Tidball JG (1983) The geometry of actin filament-membrane association can modify adhesive strength of the myotendinous junction. Cell Motil Cytoskeleton 3:439–447
Tidball JG (1987) Alpha-actinin is absent from the terminal segments of myofibrils and from subsarcolemmal densities in frog skeletal muscle. Exp Cell Res 170:469–482
Tidball JG, Daniel TL (1986) Myotendinous junction of tonic muscle cells: Structure and loading. Cell Tissue Res 245:315–322
Tidball JG, O'Halloran T, Burridge K (1986) Talin at myotendinous junction. J Cell Biol 103:1465–1472
Trotter JA, Corbett K, Avner BP (1981) Structure and function of the murine muscle-tendon junction. Anat Rec 201:293–302
Trotter JA, Eberhard A, Samora A (1983) Structural connections of muscle-tendon junction. Cell Motil Cytoskeleton 3:431–438
Trotter JA, Hsi K, Samora A, Wofsy C (1985) A morphometric analysis of the muscle-tendon junction. Anat Rec 213:26–32
Woods A, Höök M, Kjellen L, Smith CG, Rees DA (1984) Relationship of heparan sulfate proteoglycans to the cytoskeleton and extracellular matrix of cultured fibroblasts. J Cell Biol 99:1743–1753
Wright DW, Mayne R (1988) Vitreous humor of chicken contains two fibrillar systems: An analysis of their structure. J Ultrastruct Mol Struct Res 100:224–234
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Swasdison, S., Mayne, R. Location of the integrin complex and extracellular matrix molecules at the chicken myotendinous junction. Cell Tissue Res. 257, 537–543 (1989). https://doi.org/10.1007/BF00221463
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DOI: https://doi.org/10.1007/BF00221463